Do frog-eating bats perceptually bind the complex components of frog calls?

The mating calls of male túngara frogs, Physalaemus pustulosus, attract intended (conspecific females) and unintended (eavesdropping predators and parasites) receivers. The calls are complex, having two components: a frequency-modulated “whine” followed by 0–7 harmonic bursts or “chucks”. The whine is necessary and sufficient to elicit phonotaxis from females and the chuck enhances call attractiveness when it follows a whine. Although chucks are never made alone, females perceptually bind the whine and chuck when they are spatially separated. We tested whether an unintended receiver with independent evolution of phonotaxis, the frog-eating bat, Trachops cirrhosus, has converged with frogs in its auditory grouping of the call components. In contrast to frogs, bats approached chucks broadcast alone; when the chuck was spatially separated from the whine the bats preferentially approached the whine, and bats were sensitive to whine–chuck temporal sequence. This contrast suggests that although disparate taxa may be selected to respond to the same signals, different evolutionary histories, selective regimes, and neural and cognitive architectures may result in different weighting and grouping of signal components between generalist predators and conspecific mates.     

Choosing a Mate in a Cocktail Party‐Like Situation: The Effect of Call Complexity and Call Timing between Two Rival Males on Female Mating Preferences in the Túngara Frog Physalaemus pustulosus

Signal detection, recognition, and localization are hampered when multiple signalers coincide in time and space, a problem known as ‘cocktail party effect’. In many taxa, senders utter complex calls consisting of two or more elements which often vary in the ease with which they can be assessed in different signaling environments. Receivers’ selective attention to different cues may increase the probability of correctly assigning a signal to its source (localization) in face of conspecific interference. Túngara frogs, Physalaemus pustulosus, produce complex calls consisting of an initial whine, followed by zero up to seven broad‐banded, amplitude‐modulated chucks. Under ideal conditions (without interference or noise), females prefer whines followed by chucks over whines alone, but the preference is not linear; females do not discriminate between whines with one or two chucks. When whines lack chucks, call overlap elicits random responses in females, with no preference for leading calls. In this study, I explored the combined effect of call timing and call complexity on female preferences in a two‐choice paradigm—a simplification of the cocktail party scenario. I tested the hypothesis that the effect of call overlap can be reduced when the calls of one of the two rivals have chucks, specifically more chucks than those of the rival. I gave females a choice between whines alone and with chucks (one or two) presented at three time relations (alternated, abutted, and partially overlapped) and two emission orders (whine with less chucks leading and whine with more chucks leading). I found that the preference for one chuck over no chuck was preserved in all the experimental treatments, but when a w + 2chk preceded a w + chk, either overlapped or abutted, a preference existed for the whine with more chucks. Therefore, an interaction between call order and the number of chucks was obtained. The results only partially supported the hypothesis, and call order emerges as an opportunistic component of signaling in P. pustulosus.     

Modelling the production of complex calls in the túngara frog (Physalaemus pustulosus)

Relatively few studies have used experimental manipulations to investigate the mechanics of vocal production in frogs and toads, even though many frogs produce complex signals with multiple components and/or nonlinearities. Modelling approaches can add to empirical studies by illuminating how various components of the vocal system interact to produce communication signals. In this study, we use bond graphs, a lumped-element modelling technique, to explore how the combination of active modulation of vocal production and the passive dynamics of a unique laryngeal structure result in the complex calls produced by males in an anuran model system. The túngara frog (Physalaemus (= Engystomops) pustulosus) produces advertisement calls with a ‘whine’ and a facultative ‘chuck’. Whines are amplitude and frequency modulated. The chuck is characterized by its spectral complexity and appears to contain a period doubling bifurcation resulting in subharmonics. In our model, we focus on how a fibrous mass attached to the vocal cords results in subharmonics in the chuck. Our models suggest that active (neural) modulation of the fibrous mass is not necessary for the transition between the spectral characteristics of the whine and chuck. Rather, it is possible that the vibratory mode of the fibrous mass and thus the vocal cords changes passively as a result of changes in airflow through the system.     

A laryngeal fibrous mass impacts the acoustics and attractiveness of a multicomponent call in túngara frogs (Physalaemus pustulosus)

The evolution of elaborate signals can emerge from changes in anatomical signaling structures. In the male túngara frog, a simple advertisement call (‘whine’) can be ornamented facultatively with a suffix (‘chuck’) to produce a more attractive complex call, or ‘whine-chuck’. A fibrous mass (FM1) supported by the vocal cords plays a role in chuck production. Here, we examine the effects of FM1 ablation on a large set of spectral and temporal features of both the whine and chuck and we test the hypothesis that FM1 ablation reduces call attractiveness to females. Both call components were impacted by FM1 ablation, but especially the suffix. The proportion of energy in the suffix’s odd compared to even harmonics diminished markedly as did the relative amplitude, effectively eliminating the chuck percept. FM1 ablation also reduced the whine’s frequency and its rate of frequency modulation. Moreover, post-surgery chucks no longer enhanced the attractiveness of the simple call and whines also appeared to diminish in attractiveness. Together, our results demonstrate that FM1 plays a role in the production of both call components in a way that stimulates the female auditory system and that the growth of FM1 had potentially positive sexual selection implications for the pre-existing simple call.     

Signal Redundancy and Receiver Permissiveness in Acoustic Mate Recognition by the Tungara Frog, Physalaemus pustulosus

The tungara frog has an advertisement call with two structurallyand functionally distinct components: the whine is both necessaryand sufficient for species recognition, and addition of chucksfurther enhances call attractiveness. Only the fundamental frequencyof the whine contributes to phonotaxis; the upper harmonicsplay no role. Furthermore, only a small portion of the whine,within the first 0–100 msec, is necessary to elicit phonotaxis;there is some redundancy since either the 0–50 msec orthe 50–100 msec portion elicits a response. Most of theremainder of the whine's fundamental further enhances call attractiveness.Only the amphibian papilla in the peripheral auditory systemis involved in decoding the whine. In stark contrast, severalchuck variants, which stimulate either the amphibian papillaor the basilar papilla, and white noise are as effective inenhancing call attractiveness as is the normal chuck, showingthat either peripheral end organ can be involved in the perceptionof a more attractive call. Thus there is greater receiver specificityfor decoding stimuli in interspecific mate choice, and greaterreceiver permissiveness for decoding stimuli in intraspecificmate choice; it appears that intraspecific mate choice can takeadvantage of a greater array of neural pathways for call decodingthan can interspecific mate choice.     

No pre-existing biases for heterospecific call traits in the frog Physalaemus enesefae

Previous phonotaxis studies with two species of the Physalaemuspustulosus species group indicated that female preferences for several heterospecific call traits resulted from sensory biases inherited from a common ancestor. In phonotaxis experiments, we determined whether Physalaemus enesefae, a distant relative of the P. pustulosus group, showed similar preferences for call traits not present in conspecific males. We presented females with a choice between the typical conspecific advertisement call and the same call to which we digitally appended a chuck from P. pustulosus, a squawk from P. freibergi, and an amplitude-modulated prefix from P. pustulatus. In addition we presented the advertisement call in doublets, a trait peculiar to P. coloradorum. We also analysed male vocal behaviour evoked in response to the same suite of stimuli. Physalaemus enesefae females did not prefer the calls of their own males with appended heterospecific traits over unmodified calls, nor conspecific calls in doublets over single calls. The lack of preference among females was not the result of a behavioural polymorphism. Female responses to repeated presentations of the same stimulus pair were not consistent. Males also did not show an enhanced vocal response to altered calls relative to the typical conspecific call. Consequently, there are no pre-existing biases for these heterospecific call traits in P. enesefae; pre-existing preferences in the P. pustulosus group could have been inherited from an ancestor not shared with P. enesefae, but data from other closely related species are needed to confirm this conclusion. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

THE SENSORY BASIS OF SEXUAL SELECTION FOR COMPLEX CALLS IN THE TÚNGARA FROG,PHYSALAEMUS PUSTULOSUS (SEXUAL SELECTION FOR SENSORY EXPLOITATION)

Male túngara frogs (Physalaemus pustulosus) vocalize to attract females, and enhance the attractiveness of their simple, whine-only call by adding chucks to produce complex calls. Complex calls contain more total energy and are of longer duration. By virtue of the greater frequency range of the chuck, complex calls also simultaneously stimulate both the amphibian papilla and the basilar papilla of the frog's inner ear. Female phonotaxis experiments using synthetic stimuli demonstrate that an increase in the call's acoustic energy is not sufficient to account for the enhanced attractiveness of the complex call. However, the stimulation of either or both of the female's sound-sensitive inner-ear organs is sufficient to elicit her preference. We suggest that the female's sensory system generates selection that equally favors at least three evolutionary alternatives for enhancing call attractiveness and that historical constraints imposed by the male's morphology determined which of the alternatives was more likely to evolve. These data are consistent with our hypothesis of sensory exploitation, which states that selection favors those traits that elicit greater stimulation from the female's sensory system and which emphasizes the nonadaptive nature of female preference.     

Female mate choice and the potential for ornament evolution in túngara frogs Physalaemus pustulosus

The potential for ornament evolution in response to sexual selection rests on the interaction between the permissive-ness or selectivity of female preferences and the constraints on male development of signaling related traits. We investigate the former by determining how latent female preferences either exaggerate the magnitude of current traits (I.e. Elaborations) or favor novel traits (I.e. Innovations). In tungara frogs, females prefer complex mating calls (whine-chucks) to simple calls (whine only). The whine is critical for mate recognition while the chuck further enhances the attractiveness of the call. Here we use a combina-tion of synthetic and natural stimuli to examine latent female preferences. Our results show that a diversity of stimuli, including conspecific and heterospecific calls as well as predator-produced and human-made sounds, increase the attractiveness of a call when added to a whine. These stimuli do not make simple calls more attractive than a whine-chuck, however. In rare cases we found stimuli that added to the whine decrease the attractiveness of the call. Overall, females show strong preferences for both elaborations and innovations of the chuck. We argue that the emancipation of these acoustic adornments from mate recognition allows such female permissiveness, and that male constraints on signal evolution are probably more important in explaining why males evolved their specific adornment. Experimentally probing latent female preferences for stimuli out of the species' range is a useful means to gain insights about the potential of female choice to influence signal evolution and thus the astounding diversity in male sexually-selected traits.     

The effects of time,space and spectrum on auditory grouping in túngara frogs

Male túngara frogs (Physalaemus pustulosus) produce complex calls consisting of two components, a ~350 ms FM sweep called the “whine” followed by up to seven ~40 ms harmonic bursts called “chucks”. In order to choose and locate a calling male, females attending to choruses must group call components into auditory streams to correctly assign calls to their sources. Previously we showed that spatial cues play a limited role in grouping: calls with normal spectra and temporal structure are grouped over wide angular separations (≤135°). In this study we again use phonotaxis to first test whether an alternative cue, the sequence of call components, plays a role in auditory grouping and second, whether grouping is mediated by peripheral or central mechanisms. We found that while grouping is not limited to the natural call sequence, it does vary with the relative onset times of the two calls. To test whether overlapping stimulation in the periphery is required for grouping, the whine and chuck were filtered to restrict their spectra to the sensitivity ranges of the amphibian and basilar papillae, respectively. For these dichotic-like stimuli, grouping still occurred (albeit only to 45° separation), suggesting that stream formation is mediated by central mechanisms.     

SPECIES RECOGNITION AND SEXUAL SELECTION AS A UNITARY PROBLEM IN ANIMAL COMMUNICATION

We investigated patterns of mating call preference and mating call recognition by examining phonotaxis of female túngara frogs, Physalaemus pustulosus, in response to conspecific and heterospecific calls. There are four results: females always prefer conspecific calls; most heterospecific calls do not elicit phonotaxis; some heterospecific calls do elicit phonotaxis and thus are effective mate recognition signals; and females prefer conspecific calls to which a component of a heterospecific call has been added to a normal conspecific call. We use these data to illustrate how concepts of species recognition and sexual selection can be understood in a unitary framework by comparing the distribution of signal traits to female preference functions.     

Neural Activity Patterns in Response to Interspecific and Intraspecific Variation in Mating Calls in the Túngara Frog

Background

During mate choice, individuals must classify potential mates according to species identity and relative attractiveness. In many species, females do so by evaluating variation in the signals produced by males. Male túngara frogs (Physalaemus pustulosus) can produce single note calls (whines) and multi-note calls (whine-chucks). While the whine alone is sufficient for species recognition, females greatly prefer the whine-chuck when given a choice.

Methodology/Principal Findings

To better understand how the brain responds to variation in male mating signals, we mapped neural activity patterns evoked by interspecific and intraspecific variation in mating calls in túngara frogs by measuring expression of egr-1. We predicted that egr-1 responses to conspecific calls would identify brain regions that are potentially important for species recognition and that at least some of those brain regions would vary in their egr-1 responses to mating calls that vary in attractiveness. We measured egr-1 in the auditory brainstem and its forebrain targets and found that conspecific whine-chucks elicited greater egr-1 expression than heterospecific whines in all but three regions. We found no evidence that preferred whine-chuck calls elicited greater egr-1 expression than conspecific whines in any of eleven brain regions examined, in contrast to predictions that mating preferences in túngara frogs emerge from greater responses in the auditory system.

Conclusions

Although selectivity for species-specific signals is apparent throughout the túngara frog brain, further studies are necessary to elucidate how neural activity patterns vary with the attractiveness of conspecific mating calls.     

Squirrel monkey chuck call: vocal response to playback chucks based on acoustic structure and affiliative relationship with the caller

Adult female squirrel monkeys (genus Saimiri) that are socially familiar often exchange the chuck vocalization, which differs acoustically across individuals. We used behavioral observations, vocalization playback experiments, and analysis of the acoustic properties of vocalizations to investigate the effect of caller identity and acoustic structure on vocal response to playback chucks in two all-female social groups (n=10 females). Females were most likely to respond with a chuck to the playback chucks of their closely affiliated partners compared to those of nonaffiliated group members. This shows for the first time that the chuck stimulus alone is sufficient to elicit a chuck response from a female's affiliated partner. Additionally, females responded with a chuck mostly to familiar playback chucks from their own group and least to playbacks of silent controls. Unfamiliar playback chucks from the same species and a different squirrel monkey species elicited chuck responses intermediate between familiar chucks and silent controls. Post-hoc discriminant function analyses provide preliminary evidence that females are most likely to respond to unfamiliar chucks when those chucks are close in acoustic structure to familiar chucks from their own social group. These results provide a provisional explanation for error in the squirrel monkey signal processing system, in which unfamiliar chucks never heard before nevertheless elicit a chuck response if they are similar in acoustic structure to familiar group chucks.     

The Consequences for Communication of Call Overlap in the Tungara Frog,a Neotropical Anuran with a Frequency-modulated Call

We presented male tungara frogs, Physalaemus pustulosus, with call-triggered computer-synthesized whines that either did or did not overlap the frogs' own frequency-modulated whines in time. When the stimulus was nonoverlapping, males added a high proportion of chuck notes to their calls. When the stimulus was overlapping, males responded with either no or only small increases in chucking. This suggests they have difficulty detecting whines while vocalizing. When female tungara frogs were given a choice between alternating whines and out-of-phase overlapping whines they did not discriminate. The result with males was similar to that previously obtained with species of frogs that have amplitude-modulated advertisement calls (Schwartz 1987a), the result with females was different. We discuss our findings in relation to peripheral processing of spectral and temporal information in the anuran auditory system.     

Sexual Differences in the Behavioral Response of Túngara Frogs, Physalaemus pustulosus, to Cues Associated with Increased Predation Risk

Engaging in mating behaviors usually increases exposure to predators for both males and females. Anti‐predator strategies during reproduction may have important fitness consequences for prey. Previous studies have shown that individuals of several species adjust their reproductive behavior according to their assessment of predation risk, but few studies have explored potential sexual differences in these strategies. In this study, we investigate whether the acoustic cues associated with predatory attacks or those associated with predators themselves affect the mating behavior of female and male túngara frogs, Physalaemus pustulosus. We compared the responses of females approaching a mate and those of calling males when exposed to mating calls associated with sounds representing increased hazard. When presented with mating calls that differed only in whether or not they were followed by a predation‐related sound, females preferentially approached the call without predation‐related sounds. In contrast to females, calling males showed greater vocal response to calls associated with increased risk than to a call by itself. We found significant differences in the responses of females and males to several sounds associated with increased hazard. Females behaved more cautiously than males, suggesting that the sexes balance the risk of predation and the cost of cautious mating strategies differently.     

A TEST FOR ENVIRONMENTAL EFFECTS ON BEHAVIORAL ISOLATION IN TWO SPECIES OF KILLIFISH

Behavioral isolation is a common and potent mechanism of reproductive isolation. Determining the extent to which behavioral isolation varies with environmental conditions is critical to understanding speciation and the maintenance of species boundaries. Here, we tested the effect of salinity on behavioral isolation (female species recognition, male–male competition, and male species recognition) between two closely related killifish (Lucania goodei and L. parva) that differ in salinity tolerance. We performed no‐choice assays and behavioral trials where males could compete and court females in fresh water (0 ppt) and brackish water (15 ppt). We found high levels of behavioral isolation that did not vary as a function of salinity. In behavioral trials, male species recognition of females was strong and asymmetric between the two species. Lucania goodei males preferred conspecifics and rarely courted or mated with L. parva females. Lucania parva males preferred conspecifics but readily courted and mated with L. goodei females. This asymmetry matches previously documented asymmetries in hybrid offspring fitness. Crosses between L. parva males and L. goodei females produce fully viable/fertile hybrids, but crosses between L. goodei males and L. parva females produce males with reduced fertility. Hence, behavioral isolation may have evolved in part due to reinforcement.     

Call recognition and female choice in a treefrog with a multicomponent call

Acoustic mating signals are typically species‐specific, and often additionally are subject to directional female preferences. Male executioner treefrogs, Dendropsophus carnifex, produce a multicomponent advertisement call composed of an introductory screech note followed by two or more click notes. Here, we tested (i) call recognition by comparing female directed phonotaxis towards individual and combined call components: screech vs. clicks vs. screech + clicks, (ii) female preferences for greater numbers of click notes and (iii) female preferences for faster call rates. The results demonstrated that screeches and clicks, presented either separately or together as a complete call, evoke similar female responses, suggesting that either note was sufficient to elicit a mate‐recognition response. Additionally, females preferred calls with greater numbers of click notes and with faster call rates. We interpret these results within the context of female mate selection in natural choruses.     

Dual Function of Chip Calls Depending on Changing Call Rate Related to Risk Level in Territorial Pairs of White‐Eared Ground‐Sparrows

Different mechanisms have been proposed for encoding information into vocalizations: variation of frequency or temporal characteristics, variation in the rate of vocalization production, and use of different vocalization types. We analyze the effect of rate variation on the dual function of chip calls (contact and alarm) produced by White‐eared Ground‐sparrows (Melozone leucotis). We conducted an acoustic playback experiment where we played back 1 min of four chip call rates (12, 36, 60, 84 calls/min). We measured the response of territorial pairs using behavioral responses, and fine structural features of calls produced in response to those playbacks. White‐eared Ground‐sparrows showed more intense behavioral responses to higher than lower call rate playbacks. Both individuals of the pair approached the source of the playback stimulus faster, produced the first vocalization faster, produced more vocalizations, and spent more time close to the stimulus in higher call rate than in lower call rate playbacks. Frequency and duration characteristics of calls (chip and tseet) were similar in response to all call rate playbacks. Our playback experiment elicited different intensity of behavioral responses, suggesting that risk‐based information is encoded in call rate. Our results suggest that variation in the rate of chip call production serves a dual function in this species; calls are used at lower rates for pair contact and at higher rates for alarm/mobbing signals.     

INDIVIDUAL VARIATION OF THE FEMALE ATTRACTION CALL PRODUCED BY AUSTRALIAN FUR SEAL PUPS THROUGHOUT THE MATERNAL DEPENDENCE PERIOD

ABSTRACT

Australian fur seals are colonial breeding animals that give birth on crowded rookeries. Females leave their pups unattended for extended periods while they forage at sea. On return to the colony, a mother must relocate her pup amongst the hundreds of other pups. Vocal recognition is thought to play a vital role in maintaining the mother-pup bond. In the present study, four sets of 7 different pups were recorded once each at different times throughout the maternal dependence period. The Female Attraction Call was used to determine whether Australian fur seal pups produce individually distinct calls which could be used as a basis for vocal recognition. Results from three different analyses (PIC, DFA and CART) indicated that the fundamental frequency, number of parts per call, duration, quavering and peak frequency changes at the start, mid-point and end of the call (i.e., along PEAK Fl) were important to recognition. In 75% of cases using DFA, the Female Attraction Call was classified to the correct caller, suggesting that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition by females.     

一种泡蟾的配偶识别:脑、行为和进化研究

综述了对泡蟾(Physalaemuspus pustulosus)的性通讯所进行的各种研究。本文作者研究了通讯系统的功能重要性、通讯的神经机制以及通讯进化的格局,特别研究了雌蛙如何使用简单和复杂的叫声来识别可以交配的物种,以及如何识别同种的不同雄性个体。本文确定了复杂叫声的反选择力、一种食蛙蝠——缨唇蝠(Trachops cirrhosus)以及叫声的能量消耗,并阐述了引起雌性反应的重要特征。作者的比较研究表明,对复杂叫声的偏好在复杂叫声进化前就有了,这支持感官开发假说(Hypothesis of sensory exploitation,雄性特征进化的结果是开发雌性预先存在的对雄性的偏好)。结合比较研究和人工神经网络的模拟,作者认为雌蛙用来识别雄性简单叫声的解码策略受其祖先解码策略的影响[动物学报49(6)：713～726,2003]。     

Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis

The phonotactic response of cricket females was investigated on a locomotion compensator to determine the temporal parameters of the male's calling song which are important for species recognition. Two sympatric species (Teleogryllus commodus, T. oceanicus) that show different syllable periods in the chirp and trill parts of their calling songs were used. By their responses T. commodus females exhibited two temporal filters for syllable periods, which were tuned to the species-specific syllable periods occurring during chirp and trill. For song recognition both filters had to be activated and for both a minimum number of three to five consecutive syllable periods was necessary. In contrast, T. oceanicus females showed only one sharply tuned filter corresponding to the chirp part of the male's calling song. This filter was sufficient for calling song recognition. Syllable periods of the trill part also influenced calling song recognition, but these played only a minor role. Carrier frequency was also important for positive phonotaxis. Calling song recognition by T. commodus females is largely based on central nervous processing, while for T. oceanicus both peripheral frequency filtering and central temporal filtering is important. Accepted: 17 January 1997